Impact of Dynamic and Static Load on Bone Around
Implants: An Experimental Study in a Rat Model
Atsushi Yagihara, DDS1/Ryo Kawasaki, MEng1/Atsushi Mita, DDS, PhD1/Kazuo Takakuda, PhD2
Purpose: This study aimed to evaluate peri-implant bone reactions to dynamic and static loads in a rat
model. Materials and Methods: Two cylindrical titanium implants were placed in the left tibia diaphysis of
39 rats, which were divided into three groups: static load for 4 weeks (S4), static load for 8 weeks (S8), andstatic load for 4 weeks followed by dynamic load for 4 weeks (S4D4). All implants received a mechanicallateral load. After the experiment, the implants were extracted to determine the attachment strength aroundthe bone and implant. The new bone formation and bone-to-implant contact were measured using plain
and polarized light microscopy. Results: Histologic tissue analysis revealed good contact between the bone
and implant, and new bone formation around all implants. The S4D4 group had the greatest attachment
strength, new bone formation, and complex collagen fiber orientation in the new bone tissue, compared withthe other groups. No statistically significant differences in bone-to-implant contact were observed among thethree groups. Conclusions: Applying dynamic and static loads to osseointegrated implants increased theamplification of new bone. The attachment strength was significantly improved when dynamic load was used
for 4 weeks, compared with when static load was used. Int J Oral Maxillofac Implants 2016;31:e49–e56.
doi: 10.11607/jomi.4372
Keywords: animal experiment, dynamic load, implant attachment strength test, peri-implant bone, static loadInfection and overload have been described as negative factors that can cause implant loss. In addition,
recent studies have clearly indicated that infection is
the major cause of peri-implant bone resorption, andfurther studies regarding peri-implantitis are expectedin the future. However, the correlation between overload and bone resorption remains unclear.
Isidor1 has reviewed the possibility of bone resorption due to overload in experimental studies, although
the causal association between overload and bone
resorption remained unclear in the clinical studies
that were reviewed. Fu et al2 reported that periimplant damage was clearly caused by overload in
their systematic review. In addition, they described a
protocol to prevent biomechanical complications due
to overload. In contrast, many reports have concluded
that no correlation exists between overload and the

1PhD Student, Institute of Biomaterials and Bioengineering,Tokyo Medical and Dental University, Tokyo, Japan.
2Professor, Institute of Biomaterials and Bioengineering, Tokyo

Medical and Dental University, Tokyo, Japan.
Correspondence to: Dr Atsushi Yagihara, FAMILY Dental
Clinic, 5372-3 Osaki Koga Ibaraki, 306-0101, Japan.
Fax: +81-280-77-1635. Email: ayagihara@family-dent.jp
©2016 by Quintessence Publishing Co Inc.

resorption of peri-implant bone3–5; therefore, theevidence for any such mechanism remains unclear.
Brunski pointed out that dynamic load in a physiologically tolerated range enhanced bone remodeling.6
Interestingly, two primary studies have indicated thatbone resorption due to overload is likely induced byinflammation, such as dental plaque.7,8 However, theauthors also mentioned the possibility of overloadcausing an increase in the peri-implant bone density
when plaque is adequately controlled. Furthermore,
Qian et al4 clearly stated that they found no evidence
that early peri-implantitis may be induced by overload
alone, although they also stated that peri-implantbone resorption was induced by intricate combinations of multiple factors, such as the implant hardware,clinical handling, and patient characteristics. Similarly, Rungruanganunt et al5 reviewed 36 publications(including clinical and animal studies), and reported
that the impact of static load was related to misfit of
the superstructures. These authors also mentionedthat static load alone clearly did not negatively impact
the implant’s survival.
Intraoral loading designs are broadly divided into
dynamic load7,8 (such as occlusal load) and continuously static load,9 which is associated with incompatibility of the superstructures. Therefore, it is very
important to compare these types of overload when
considering the occlusal style. Although many studies
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Yagihara et alreported the effect of dynamic load alone (such as
occlusal load in animals), or mechanically applied
static load alone, on the peri-implant bone, few animalstudies have compared both dynamic and static loads.
Among these studies, Duyck et al10 compared staticand dynamic loads in rabbit tibias, and reported thatsignificant resorption of the peri-implant bone was
detected in the dynamic load group compared withthat in the static load group, although no significant
difference in the bone-to-implant contact ratio (BIC)
was observed. Therefore, it appears that the lack ofconsensus regarding the correlation between implantloss and load is related to (1) the lack of a standardized
implant design when evaluating overloading and(2) few studies having assessed standardized quantitative dynamic and static loads.
In recent years, most commercial implants havebeen the screw type (with threads), and these provide
a superior initial fixation.
However, when measuring the attachment strength
between the bone and implant, it is difficult to distinguish between osseointegration and the mechanicalfitting force, as significant resistance may be related
to the screw fit, even if osseointegration is absent.
In addition, clinical reports have stated that implantloss is most common in the first year after surgicalplacement.11 Although these reports have indicatedthat a history of periodontitis was the main causal
factor, it is also possible that the implants did notachieve osseointegration due to technical difficulties
that were encountered by the surgeon. For example,
most implants can survive for several months simply
because of the mechanical fit between the screw andbone. In addition, the period between implantationand osseointegration is shorter in rat models than in
humans; therefore, it is very difficult to clearly identify
real osseointegration. Several methods are available
to confirm completed osseointegration, although theevidence is reportedly limited for all of these methods.12 Therefore, most basic osseointegration should
be judged using mechanically polished, straight titanium implants.
Many studies have reported overload due to occlusal load in animals and humans, and these models arefavorable because they closely mimic the clinical style.
However, it becomes difficult to objectively define
the quantitative load and cycle that is administered.
Furthermore, animal occlusal models require large
animals, such as dogs and monkeys, making it difficult to incorporate large experimental groups, andresulting in highly variable mean values. Therefore, it
is important to quantitatively assess the load protocol
as a numerical value, rather than as an ambiguously
qualitative load, and these specific numerical values​​
would be helpful for future studies.

In this study, the authors constructed a basic rat tibial
model to assess the peri-implant tissue morphology
and attachment strength when a quantitative load wasapplied to well-osseointegrated, mechanically polished,straight titanium implants. In this model, the authorscarefully ensured secure osseointegration, and completely
eliminated inflammation and infection, which allowed
them to evaluate only the bone’s reaction to overload.

MATERIALS AND METHODS
Animals and Surgical Procedures

Thirty-nine Sprague-Dawley rats (12 weeks old, mean
body weight: 450 ± 20 g) were used in this study. These
rats were divided into three groups: static load for 4 weeks(S4), static load for 8 weeks (S8), and static load for 4 weeks
followed by dynamic load for 4 weeks (S4D4). Eight weeks
after the implant placement, all rats were sacrificed via
a lethal overdose of intravenous sodium pentobarbital.
The experiments were conducted in compliance withthe animal care guidelines laid out by the National Institutes of Health (NIH) and the institutional animal care
committee of Tokyo Medical and Dental University. This
study protocol was also reviewed and approved by theinstitutional animal care committee (0130200A).

Implant Placement

Two cylindrical, 99.5% commercially pure, titanium
implants (diameter: 1.5 mm, length: 40 mm, Nillaco) wereused for each rat. Before the placement, the experimental
implants were degreased with acetone, rinsed with 70%
ethanol, rinsed again with distilled water, dried at room
temperature, and sterilized in an autoclave. The animals
were then anesthetized using isoflurane (Isoflu, Abbott
Laboratories), and a periosteal separation was made on
the left medial side tibia to expose the bone. Two parallel
implant holes (diameter: 1.6 mm) were drilled using a
low-speed hand drill (Kyocera). All implants were placed
bicortically, with both ends exposed approximately 10 mmoutside of the skin, and the incision was subsequently
closed with 6-0 nylon sutures. A healing phase of 4 weeks
was set to complete osseointegration.

Static Load Device

The devices10,13 for static loading were prepared by
mounting four 0.98-N super elastic springs (TOMY), as
shown in Fig 1. The two implants were connected to eachother at both sides, which allowed a continuous staticload of 3.92 N to be exerted.

Dynamic Load Device

The dynamic load was set using the following parameters:
1,800 cycles, 3.92 N amplitude, and 3 Hz frequency. An
electromagnetic microtester (MMT-250N Shimadzu) was

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Yagihara et al

ST

Ti

Ti
UG

TB

TB
Ti
Ti

LG
ST

Fig 1   The experimental device for static loading. A total of four
springs were mounted between the implants. Ti = titanium implant; TB = tibial bone; ST = soft tissue; Arrow = a 0.98-N superelastic open spring.

Fig 2   The experimental device for dynamic loading. Both endsof two implants were fixed by the device. Ti = titanium implant;
TB = tibial bone; UG = upper grip; LG = lower grip; ST = soft tissue; Arrow = loading direction.

also used. For the dynamic load experiment,10,13 each
implant was fixed to the device for 10 minutes each day,as shown in Fig 2, and the actuator was used to apply
the load to the implant. This loading was performed 5days per week, over a total of 4 weeks.

under a polarized light microscope, and the average
thickness of the hypodermal tissues was determined in
the tissues adjacent to the implant (radius: –500 μm).
Furthermore, the new bone formation ratio (NBF) was
estimated using the bone tissue on the implant surface.
BIC = Bone contact length (pixel)/Total length (pixel)
NBF = New bone area (pixel)/(New bone area + existing bone area) (pixel)

Histologic Observations

Four weeks (S4) and 8 weeks (S8, S4D4) after the implant
placement, all rats were sacrificed via a lethal overdoseof sodium pentobarbital. Eighteen tibial cortical blockspecimens (S4: six specimens, S8: six specimens, S4D4:
six specimens) of 20 mm around the implants were thendissected, and the soft tissue was removed from the bone.
For histologic observation, the implants and surrounding
bone tissues were fixed in 10% formalin immediately
after harvesting. The samples were then dehydrated ina graded series of ethanol, defatted using xylene, andembedded in methyl methacrylate resin (Osteoresin,Wako). Thin sections (approximately 70 μm thick) werethen prepared using a diamond disc microtome (SP1600,
Leica Microsystems).
These sections were then stained with toluidine blue
and observed under a light microscope (Eclipse 50i, Nikon)that was equipped with a digital camera (Digital Sight
DS-SM5, Nikon). Quantitative morphologic evaluation of
the histologic sections was also performed, and the lengthof the direct contact between the bone and implant (BIC)
was measured. In addition, the sections were observed

Evaluating Attachment Strength

To evaluate the mechanical attachment strength between
the implant and bone, 19 tibias (S4: six samples, S8: six
samples, S4D4: seven samples) were evaluated using amaterial testing machine (Autograph AG-X, Shimadzu).
The testing was performed at a crosshead speed of 5 mm/
minute, and the load and displacement data were recorded in a computer. Using these data, the maximum force
value was considered to be the attachment strength.

Statistical Analysis

All data were expressed as mean ± standard deviation,
unless otherwise stated. The mechanical strength test
results, BIC, and NBF were statistically analyzed using
Welch’s t test with Holm’s correction for multiple comparisons. All statistical analyses were performed using“R” software (http://www.r-project.org/), and differenceswere considered statistically significant if the P value
was < .05.
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Yagihara et al

Fig 3 (left)  A tibia dissected for histologic evaluation after
cutting the extra-implant ends. Implants were fixed firmly, withhealthy bone.
Fig 4 (below)  Light microscopy observations using toluidine
blue stain. (a) An axial cross section of the implant. (b) A horizontal cross section of the implant. The implant and surrounding
bone have good contact, and amplification of the bone is foundoutside of both cortical bones. Ti = titanium implant; C = cortical bone; BM = bone marrow.

C

C
BM

Ti

BM
Ti

a

b

RESULTS
During the experimental period, the general condition of the rats and the tissues surrounding theimplants were examined every day. At 4 weeks after
the implant placement, two rats’ implants had not
developed osseointegration; therefore, they were
excluded from the analysis. Based on this exclusion,
the S4 and S8 groups included 12 rats, while the S4D4group included 13 rats. However, after osseointegration, amplification was observed in the tibial bonesurrounding the implants for all remaining samples(Fig 3).

The results of the BIC comparison are shown in Fig
7a, and approximately 50% bone contact was observedin all three groups. The BIC was 50.4% ± 34.8% in
the S4 group, 44.3% ± 20.7% in the S8 group, and50.9% ± 23.7% in the S4D4 group; these differenceswere not statistically significant.
The results of NBF comparison are shown in Fig
7b, and approximately 10% to 20% new bone wasobserved in the three groups (vs the preexistingbone). Specifically, the NBF value was 10.6% ± 4.10%
in the S2 group, 11.9% ± 3.55% in the S8 group, and17.1% ± 3.35% in the S4D4 group. Significant differences were observed between the S4D4 and S8groups, and between the S4D4 and S4 groups.

Histologic Observation

Measuring Mechanical Strength

Macroscopic Observation

Toluidine blue–stained tissue samples were observed
via plain light microscopy (Fig 4), and the BIC between
the implant and bone was measured (Fig 5). Polarized
light microscopy was used to evaluate the NBF (Fig 6),
and bone formation was observed inside and outside
the bone in all samples from each group. The collagen fibers ran regularly inside the bone for all groups,
although irregular collagen fibers were clearly visible
in the new bone area; these changes were used todefine the new bone and calculate its area.

The result of the mechanical strength tests were
10.4 ± 4.81 N in the S4 group, 16.1 ± 7.35 N in the
S8 group, and 28.9 ± 12.7 N in the S4D4 group (Fig7c). Based on these values, a significant difference
was observed between S4 and S4D4, and between
S8 and S4D4 (both P < .05), although no significant
difference was observed between S4 and S8. These
results revealed a trend whereby the strength of theosseointegration increased when dynamic load wasapplied to the osseointegrated implant.

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Yagihara et al

PB
C

BM

500 µmTia

500 µm

NB

Ti

a

W

C

NB

500 µmTib

PB

500 µm

C

Ti

b

PB

BM
NB
500 µm500 µm

a

60
50
40
30
20
10
0
S4

S8

S4D4

New bone formation ratio (%)

Bone-implant contact (%)

Fig 5   Light microscopy observations using toluidine blue stain.
(a) S4, (b) S8, and (c) S4D4. The bone-to-implant contact ratio
was measured using these samples, and the bone surrounding
the implant exhibited good osseointegration for all the groups.
Ti = titanium implant; C = cortical bone; BM = bone marrow; redline = bone contact length; yellow line = total length.

b

Fig 6  Polarized light microscopy observations using toluidine
blue stain. (a) S4, (b) S8, and (c) S4D4. The new bone formation
ratio was measured using these samples. Collagen fibers ran
regularly in the preexisting bone for all groups, compared withirregularly in new bone. Fibers that were closer to the periphery of the implant ran more parallel in the S4 and S8 groups,
whereas the pattern was mostly irregular in the S4D4 group,
ranging from oblique to almost perpendicular. Ti = titanium implant; NB = new bone; PB = preexisting bone.

*

20

Ti

c

*

15
10
5
0
S4

S8

S4D4

Attachment strength (N)

Ti

c

*

40

*

30
20
10
0
S4

S8

S4D4

c

Fig 7   Bone-to-implant contact ratio (BIC), new bone formation (NBF) ratio, and attachment strength. (a) BIC (S4, S8, and S4D4:
n = 6). No significant differences in BIC were observed among the three groups. (b) NBF (S4, S8, and S4D4: n = 6). *Significant
differences were observed between S4 and S4D4, and between S8 and S4D4 (P < .05). (c) Attachment strength (S4 and S8: n = 6;
S4D4: n = 7). *Significant differences were observed between S4 and S4D4, and between S8 and S4D4 (P < .05).

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Yagihara et al

DISCUSSION
Many different research designs (eg, animal experiments,7,8 clinical studies,14 and finite element analyses15
have been used to investigate the effects of load on
implant status, and these studies have evaluated staticload,16 dynamic load,17 occlusal load of arch18 or tibiaload,19 and various load timings.20 However, their results
are conflicting, as several groups have reported a clear
correlation between overload and peri-implant bone
resorption, while others have reported no correlation
between these factors. Therefore, the aim of this study
was to assess the effect of different load types on
osseointegrated implants, and the present study is thefirst report to directly and quantitatively compare staticand dynamic loading using histologic and attachment
strength assessment.
In the literature, several groups have reported that
occlusal overload may increase bone density when plaqueis well controlled.3–5 The results of the present study support their conclusion that the loss of an osseointegrated
implant is not directly caused by overload alone. However,their conclusions were based on various load types andanimal sizes, as well as the use of occlusal loads (which
are preferable when considering clinical situations).
Furthermore, their data were qualitative, rather thanquantitative; therefore, it is difficult to directly replicate
their experiments and provide a direct comparison of theresults. Thus, the authors of the present study selected
quantitative measurements to assess the load and frequency, rather than the magnitude of the occlusal load,
which is typically evaluated using qualitative methods.
Very few study designs have attempted to quantify
dynamic load.10,21 However, Hattori et al22 have reported
that the mean number of occlusal contacts is 26.1 sites
in humans, that the mean magnitude of the occlusal
force resultants is 776.7 N, and that the mean occlusal
force magnitude on each occlusal contact is 26.2 N. In
addition, Duyck et al10 applied a static load of 29.4 N
and a dynamic load of 14.7 N to rabbit tibias in theirpreliminary experiments. In contrast, the authors of thepresent study used rats, which are smaller than rabbits, toensure an ample load could be applied, even comparedwith those used in the previous studies.
In this study, the authors hypothesized that overloadon healthy osseointegrated implants could not be
the only cause of implant loss. Therefore, they usedthreadless, mechanically polished, straight implants toeliminate any mechanical fit, which would allow them tofocus exclusively on osseointegration. They actually did
not observe any bone resorption for the implants thatexhibited complete osseointegration and healthy periimplant tissue. It should also be noted that, although ascrew implant and straight one differ in their shape, theyshared similar osseointegration processes, since both of

the bone-implant interfaces were mainly subjected to
the normal loads.
Using these experimental methods, dynamic loads
were applied immediately after implant placement as apilot study to investigate the effects on the peri-implantbone. In that study, inflammatory cells and soft tissues
appeared all around implants at approximately 4 weeks,
and none of the implants developed osseointegration,
because of the poor initial fixation. In contrast, the S4,
S8, and S4D4 groups (which were allowed to develop
adequate initial fixation) developed adequate osseointegration. These results indicate that immediate loadingof the implant (eg, when using threadless implants)
may prevent initial fixation, thereby markedly inhibiting
osseointegration. Similarly, a review by Esposito et al23
concluded that a high insertion torque value and initial
fixation are important factors for immediate loading of
implants. Therefore, mechanical fit and osseointegrationmust be clearly differentiated in loading experiments,
as initial fixation is one of the most important factors
for achieving osseointegration.
No previous study has reported a mechanical strength
resistance model using mechanically polished straighttitanium implants as a method for assessing dynamic
and static loads. In this study, the authors measured
the attachment strength between these implants andbone in the S4, S8, and S4D4 groups, and observed
significant differences between the S4D4 and S4 groups,
and between the S4D4 and S8 groups (both P < .05).
However, no significant difference was observed
between the S4 and S8 groups. These results indicatethat the bone around an implant reacts more strongly
to dynamic load, compared with the reaction to staticload. Baker et al24 conducted a similar experiment using
mechanically polished straight implants that were placed
in rabbit tibias, and they reported a mean resistance forceof 33.3 N, which is similar to the results of the present
study. However, Zheng et al25 reported a resistance of> 300 N for a microscrew implant that was placed inbeagles’ jawbones for 8 weeks, which is much higher
than the results of the present study. This discrepancy
is likely attributable to the use of a screw implant, which
provided a superior mechanical fit. Moreover, they used
the jawbone of a beagle, which has a greater quantityof bone compared to a rat tibia, and this may also havecontributed to the higher resistance. The authors of thepresent study suggest that the degree of the attachment strength between the implant and bone should
be assessed quantitatively in an experimental model
without any mechanical fit. From a clinical perspective,
and based on these findings, it is highly possible that theocclusal force in the healthy oral environment contributes
to amplification of peri-implant bone.
When considering the direction of the load, moststress is born on the neck of the implant, and bonee54 Volume 31, Number 3, 2016
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Yagihara et al

microfractures typically occur in this region.15 In addition, the lateral and oblique mechanical stress is greaterthan that exerted on the axis.26 In this context, chewing
stress frequently adds axial, lateral, and oblique loads
to oral implants. Thus, lateral loads were intentionallyapplied in the present study, which resulted in new boneamplification around the implant, rather than implantloss. In the future, the authors plan to investigate theeffects of oblique loads in an additional study.
Interestingly, the authors did not observe any significant difference in BIC between the three groups.
However, the average BIC of 48.3% in the present study
is similar to that reported in several previous studies.27
This result indicates that there is no histologic change
in the peri-implant bone, regardless of whether several
loads are applied over 4 to 8 weeks. Similar to the resultsof the present study, many experimental studies havefound no significant difference in BIC, regardless of theload type or loading time.7,10 In contrast, several otherreports have indicated a significant difference in BIC,
due to loading time, between the load and no-loadgroups.18,28 Therefore, further standardization in termsof experimental design is needed to provide reproducible experimental results.
Regarding NBF, the authors of the present study
observed a significant difference between the S4 andS4D4 groups, and between the S8 and S4D4 groups(both P < .05). Although various designs have beenused to evaluate bone amplification via polarized lightmicroscopy, no significant change in the BIC and NBFof peri-implant tissues, regardless of the load type,was observed in one study.29 Although that finding
contradicts the results of the present study, further
detailed studies are needed, given the limited numberof quantitative reports.
Based on the collagen fibers’ orientation, the polarized light microscopy analysis in the present study
revealed notable difference in the new bone’s properties. Interestingly, previous studies have reported
that collagen fibers were oriented perpendicular or
oblique to the direction of the load.30–32 In addition,bone regeneration and collagen fiber orientation arelikely related, regardless of the implant material orits surface properties.33,34 In this study, the collagenfibers’ orientation depended on the type of load that
was applied. For example, the collagen fibers ran more
oblique or perpendicular in the S8 group, comparedwith the fibers in the S4 group. In addition, the pattern
was more complicated in the S4D4 group than in the S8group. Furthermore, despite the absence of a significant
difference in the BIC, the dynamic load group exhibited
significantly greater mechanical strength resistanceand NBF. Therefore, based on these results, it appears
that the orientation of collagen fiber in new bone likely
contributes to its mechanical strength.

CONCLUSIONS
Within the limitations of this study, the application of
dynamic and static loads to a smooth osseointegrated
titanium implant in a rat tibia did not affect the periimplant bone resorption. New bone amplification was
histologically observed around all the implants after
osseointegration was achieved, and the attachment
strength and NBF were significantly increased after applying dynamic load for 4 weeks. However, no differences
in bone histologic structure were observed in the BIC
when dynamic or static loads were applied. These results
suggest that dynamic loading of implants may provide
superior mechanical and tissue benefits, compared withstatic loading or no loading.

ACKNOWLEDGMENTS
The authors report no conflicts of interest related to this study.

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